A multifunctional organelle coordinates phagocytosis and chlorophagy in a marine eukaryote phytoplankton <i>Scyphosphaera apsteinii</i>

Mixotrophy via phagocytosis can have profound consequences for the survival of marine phytoplankton and the efficiency of carbon transfer in marine systems. Little is known about the cellular mechanisms that underly nutrient acquisition via prey uptake and processing in mixotrophic phytoplankton. We used confocal microscopy, flow cytometry, and electron microscopy to assess phagocytosis and intracellular prey processing in the diploid calcifying coccolithophore Scyphosphaera apsteinii. Bioinformatic analysis was performed to develop a working model of the pathways that likely converge to regulate mixotrophic nutrition and autophagy. We found cells ingested proxy (up to 2 μm diameter) and natural (bacteria and cyanobacteria) prey particles that are processed within a single, prominent acidic vacuole detected in 80-100% of cells during exponential growth. This organelle was constitutive in cells through all growth phases to late stationary and is inherited when cells divide. Chloroplast fragments localized to this digestive organelle. A distinct, nonacidic vacuole containing polyphosphate was also identified in cells with ingested particles. We conclude a novel acidic organelle plays a multifunctional catabolic role in both mixotrophic nutrition (phagotrophy) and autophagy (chlorophagy). This discovery illustrates the dynamic nutritional strategies that marine phytoplankton, such as coccolithophores, have evolved to acquire and conserve nutrients.